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AOBPreview originally published online on October 7, 2007
Annals of Botany 2007 100(7):1459-1465; doi:10.1093/aob/mcm244
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© The Author 2007. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For Permissions, please email: journals.permissions@oxfordjournals.org

Distribution and Translocation of 141Ce (III) in Horseradish

Xiaoshan Guo1,2, Qing Zhou3, Tianhong Lu1, Min Fang1 and Xiaohua Huang1,2,*

1 College of Chemistry and Environmental Science, Nanjing Normal University, Nanjing 210097, P. R. China
2 School of Chemistry and Materials, Southern Yangtze University, Wuxi 214122, P. R. China
3 The Key Laboratory of Industrial Biotechnology, Ministry of Education, Southern Yangtze University, Wuxi 214122, P. R. China

* For correspondence. E-mail wxxhhuang{at}yahoo.com

Received: 27 March 2007    Returned for revision: 30 April 2007    Accepted: 6 August 2007    Published electronically: 7 October 2007


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
 LITERATURE CITED
 

Background and Aims: Rare earth elements (REEs) are used in agriculture and a large amount of them contaminate the environment and enter foods. The distribution and translocation of 141Ce (III) in horseradish was investigated in order to help understand the biochemical behaviour and toxic mechanism of REEs in plants.

Methods: The distribution and translocation of 141Ce (III) in horseradish were investigated using autoradiography, liquid scintillation counting (LSC) and electron microscopic autoradiography (EMARG) techniques. The contents of 141Ce (III) and nutrient elements were analysed using an inductively coupled plasma-atomic emission spectrometer (ICP-AES).

Results: The results from autoradiography and LSC indicated that 141Ce (III) could be absorbed by horseradish and transferred from the leaf to the leaf-stalk and then to the root. The content of 141Ce (III) in different parts of horseradish was as follows: root > leaf-stalk > leaf. The uptake rates of 141Ce (III) in horseradish changed with the different organs and time. The content of 141Ce (III) in developing leaves was greater than that in mature leaves. The results from EMARG indicated that 141Ce (III) could penetrate through the cell membrane and enter the mesophyll cells, being present in both extra- and intra-cellular deposits. The contents of macronutrients in horseradish were decreased by 141Ce (III) treatment.

Conclusions: 141Ce (III) can be absorbed and transferred between organs of horseradish with time, and the distribution was found to be different at different growth stages. 141Ce (III) can enter the mesophyll cells via apoplast and symplast channels or via plasmodesmata. 141Ce (III) can disturb the metabolism of macronutrients in horseradish.

Key words: Horseradish, Armoracia rusticana, cerium, 141Ce (III), translocation, distribution, radioisotope tracer technique


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
 LITERATURE CITED
 
From the 1970s onwards, it was found that the yield and quality of crops such as wheat, rice, maize, mungbean, and many others could be significantly improved using rare earth microfertilizers (Buckingham et al., 1999; Diatloff et al., 1999; Hong et al., 2000). It was well known that a large amount of these rare earth elements (REEs) entered the environment and foods, leading to environmental contamination and the accumulation of the REEs in the food chain (Volokh et al., 1990). Thus, many papers have reported the environmental and ecological effects of REEs (Markert and Li, 1991; Tyler, 2004; Huang et al., 2005). However, the biochemical behaviour of REEs in the soil–plant system is still not fully clear.

The distribution of the REEs in plant cells has been investigated in order to understand the biochemical behaviour of the REEs in the soil–plant system (Xu et al., 2002; Showler et al., 2006; Tagami and Uchida, 2006; Shtangeeva and Ayrault, 2007). However, there is very little information about whether rare earth ions can enter into plant cells and, if so, how they are distributed within them. In addition, as the concentrations of REEs are generally very low in different plant organs, conventional analytical methods have not been able to provide the desired sensitivity and accuracy. It has been reported that the radioisotopic tracing technique can be used to analyse the distribution and translocation of metal ions in the whole plant (Lin et al., 1995; Tausz et al., 2003; Bystrzejewska-Piotrowska and Urban, 2004; Mosquera et al., 2006) and the passage of ions across membranes in intact cells, synaptosomes and related systems (Lukas and Cullen, 1988; Villarroya et al., 1998; Fitch and Daly, 2005). Furthermore, the autoradiographic technique could be applied in order to obtain imaging of the uptake, translocation and distribution of radioisotopes (Mäkelä et al., 1996; Soudek et al., 2006). In addition, liquid scintillation counting (LSC) is an effective technique for the determination of radionuclides, because of high counting efficiency, easy sample preparation and easy automatization (Gómez Escobar et al., 1996). Thus, using radioisotopes of REEs as tracers is potentially a good way to study the behaviour of REEs in plants.

Horseradish (Armoracia rusticana) is a perennial herb of the cruciferae family, native to central and south Europe and naturalized in many parts of North America. In this paper, the translocation and distribution of 141Ce (III) in horseradish were investigated, together with the effect of 141Ce (III) on the uptake of macronutrients such as K, Ca and Mg, by using autoradiography, LSC and electron microscopic autoradiography (EMARG) techniques. The aim of the study was to provide valuable information towards understanding the effects of REEs on plant growth, environmental toxicology and food safety.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 CONCLUSIONS
 LITERATURE CITED
 
Preparation of radioactive cerium solution
141CeO2, as pale yellow powder, was supplied by Beijing Atom High Tech Co., Ltd in China. Its specific radioactivity concentration was 3·7 x 106 Bq mg–1 and its radiochemical purity was greater than 95 %. Prior to use, it was chemically transformed with H2O2 and HNO3 into 141Ce (NO3)3 form as follows:


Formula

Then, 1·1 mL of the 141Ce(NO3)3 solution was diluted to 15 mL with H2O. The diluted solution with 2·4 x 108 c.p.m. mL–1 specific radioactivity was used for the experiments.

Plant culture and treatments
Horseradish, Armoracia rusticana, was grown in a glasshouse at 20–25 °C and a 16-h photoperiod with 300 µmol m–2s–1 irradiance. The horseradish was planted in plastic pots in the middle of March. The diameter of the plastic pot was 40 cm and three plants grew in each pot.

When the horseradish had reached a mature stage, 1 mL of the diluted solution of 141Ce (III) was daubed on a leaf surface of each treated plant (25 October). This leaf is referred to as the labelled leaf, and the other leaves and organs without the treatment of 141Ce (III) are referred to as the unlabelled organs. Three pots of horseradish samples were harvested on 1, 2, 8 and 16 days after the treatment with 141Ce (III). Samples of the leaves, leaf-stalks and roots from one pot were collected for autoradiography analysis, and the other two pots were used for radioactive determination, in which three samples were collected from the different plants in the pots.

Autoradiography analysis of translocation of 141Ce(III)
The samples of leaves, leaf-stalks and roots of 141Ce (III)-teated horseradish were cut, washed with non-radioactive Ce(NO3)3 solution in order to prevent 141Ce (III) from diffusing out in the organs, and then washed with EDTA solution. Then, the samples were pressed between two filter papers and dried at 70 °C for 8 h. The samples were transferred to a Valumax cassette (24 x 30 cm) and put on X-ray monitoring film. The film was exposed for different durations of time depending on the type of nuclide, and then developed.

Determination of radioactivity of 141Ce(III)in different organs
The samples of the leaves, leaf-stalks and roots were cut and then washed with non-radioactive Ce(NO3)3 solution and EDTA solution as above. The samples were dried overnight at 70–80 °C and ground to a fine powder. A 20-mg sample of the powder was placed into a LSC vial, digested in 100 µL HNO3/HClO4 (5 : 1 v/v) and 200 µL H2O2 and incubated at 70–80 °C for 30–45 min. Then 5 mL of hydrophilic scintillating solution [5 g of PPO (2,5-diphenyloxazole), 665 mL xylene and 335 mL ethylenediethanol ether] were added into the vial and mixed thoroughly using a vortex for 30 min. Finally, the radioactivity of the sample was determined using a liquid scintillation counter (Beckman LS-6500). The radioactivity of each sample was calculated using the calibration of sample quenching, radioactive decay and background. The background value was the radioactivity of the hydrophilic scintillating solution.

Each sample was repeated three times, and average values are given here. The mean deviation of the radioactivity measurements was about 0·5 %.

EMARG of 141Ce(III)
Young horseradish leaves were treated with 141Ce (III) for 8 d. The leaf was then cut as a regular section of 1·5 x 2 mm size, and as an ultra-thin section of approx. 60 nm for the electron microscope observation (Reichert Ultracut E ultramicrotome). Nuclear emulsion (Technical Institute of Physics and Chemistry, Chinese Academy of Science) was painted on the leaf section and, following development and fixation, the distribution of rare earth ions could be observed using an electron microscope (Feig and Harting, 1992). The leaf sections for TEM measurements were prepared according to the method of Santos et al. (2004), and images were observed with a H-600 TEM (Hitachi Company, Japan).

Measurement of content of macronutrients (K, Ca, Mg) in roots
The roots of horseradish that had been treated with 141Ce (III) were cut and washed with triple-distilled water. The cut roots were dried overnight at 70–80 °C and ground to a fine powder. A 0·5-g sample of the powder was digested in a Microwave Digestion System CEM 2000 in a closed Teflon bomb according Chojnacka et al. (2004). The reagent composition and digestion conditions were chosen in order to achieve complete mineralization and decomposition of the solid phase into the liquid phase. After digestion, the solution was adjusted to 50 mL with triple-distilled water. The macronutrient contents (K, Ca, Mg) of digested samples were determined by ICP-AES.

The experimental data were analysed using a LSD test (at P < 0·05).


   RESULTS AND DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
CONCLUSIONS
 LITERATURE CITED
 
Figure 1 shows normal photographs and autoradiographic images of leaf-stalks connected to labelled leaves, together with the corresponding radioactivities on the different days. On the 2nd day, the colour of the top of the leafstalk was brighter than that of the bottom (Fig. 1A), indicating that 141Ce(III) can move along the leaf-stalk. The whole leafstalk was bright on the 8th day but became dark by the 16th day, suggesting that most 141Ce(III) can move to other organs via the leaf-stalk after 8 d. The change in the corresponding radioactivity (Fig. 1B) was consistent with that of the autoradiographic images. These results strongly suggested that 141Ce(III) can be absorbed in the leaf and then moved to other organs over time in horseradish.


Figure 1
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  		FIG. 1. (A) Normal photogranphs (top) and autoradiographic images (bottom) of leaf-stalks connected to the labelled leaf of horseradish on different days, and (B) a plot of the corresponding radioactivity vs. time.

 
Figure 2 shows normal photographs and autoradiographic images of unlabelled organs, and plots of the corresponding radioactivity on the 2nd and 8th days. It can be seen that almost no autoradiographic images were observed in the unlabelled organs 2 d after the treatment, indicating that very little 141Ce(III) moved from the labelled leaf to other organs in this time. However, 8 d after the treatment with 141Ce(III), the radioactivities of the unlabelled organs were clearly higher than the background (Fig. 2C), suggesting that some 141Ce(III) had been moved from the labelled leaf to the other organs in this time. On the 16th day, every unlabelled organ produced autoradiographic images (Fig. 3A) and high radioactivity (Fig. 3B), indicating that large amounts of 141Ce(III) had been moved to these organs. These results demonstrated that the distribution of 141Ce(III) in unlabelled organs changed with the time, thus illustrating the transfer of 141Ce(III) within horseradish.


Figure 2
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  		FIG. 2. (A) Normal photographs (top) and autoradiographic images (bottom) of unlabelled organs of horseradish on day 2, and plots of the corresponding radioactivity in each organ on (B) the 2nd and (C) the 8th day after treatment.

 


Figure 3
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  		FIG. 3. (A) Normal photogranphs (top) and autoradiographic images (bottom) of unlabelled organs of horseradish and (B) a plot of the corresponding radioactivity in each organ on the 16th day after treatment.

 
It can be seen from Fig. 2C and Fig. 3B that the radioactivity in the root was the highest among all the organs, while the radioactivity in leaf-stalk was higher than that in the leaf. Thus, it was evident that 141Ce(III) had uneven distribution within horseradish and its content showed the following order: root > leaf-stalk > leaf.

In order to further examine this phenomenon, the radioactivities and uptake rates of 141Ce (III) in the different organs at different times were determined (Table 1). It was found that the radioactivities of 141Ce (III) in the different organs differed at any given time. For example, the radioactivity in the labelled leaf on the 2nd day was approx. 1·10 x 108 cpm, whereas it was approx. 1·70 x 106 cpm in the leaf-stalk connected to that leaf. The radioactivities of 141Ce (III) in the unlabelled roots, leaf-stalks and leaves were 2·60 x 104, 1·80 x 104 and 9·00 x 103 cpm, respectively. The radioactivities in the unlabelled organs on the 16th day were higher than those on the 2nd day, and had the following values (in descending order): 5·10 x 106 cpm for the unlabelled roots; 2·80 x 106 cpm for the unlabelled leaf-stalks; 1·70 x 106 cpm for the unlabelled leaves; and 1·30 x 106 cpm for the leaf-stalks connected with the labelled leaves. These results indicate that 141Ce (III) has clearly been absorbed by horseradish and then moved from the labelled leaf to the unlabelled organs.


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  		TABLE 1. Absorption of 141Ce in horseradish

 
The radioactivities of 141Ce(III) in the labelled leaves and the leaf-stalks connected with them reached maximum values between the 2nd and 8th days, and then they decreased to low levels due to the translocation of 141Ce(III). The 141Ce(III) uptake rates of the unlabelled organs increased with time. On the 2nd day, the maximum uptake rate of the labelled leaf was 45·8 % and then it decreased significantly with time (Table 1). Meanwhile, the uptake rates of the unlabelled organs increased to some extent. Therefore, it can be concluded from the results that the distribution of 141Ce(III) in horseradish varied between different organs and with time.

The radioactivities of developing and mature unlabelled leaves and leaf-stalks of horseradish on the 8th and 16th day are shown in Fig. 4. It can be seen that the radioactivities in developing leaves and leaf-stalks are higher than those in mature leaf and leaf-stalks. The reason is not clear, but it may be because the translocation of 141Ce(III) is related to the metabolism of the plant. The metabolism of the developing parts of the plant is fast, and thus 141Ce(III) would transfer quickly from the labelled leaf to the developing leaf. Buchanan et al. (2000) have suggested a similar reason for such observations.


Figure 4
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  		FIG. 4. The radioactivities recorded in developing and mature unlabelled leaves of horseradish on (A) the 8th and (B) the 16th day after treatment.

 
Figure 5 shows electron microscopic autoradiographs of 141Ce(III) in horseradish cells. It can be seen that 141Ce(III) (as indicated by black/silver grains) is mainly distributed outside the cell and on the cell wall, and only small amounts of 141Ce(III) exist on both sides of plasmodesma. Figure 5B shows that 141Ce(III) is largely distributed in the cytoplasm and plasmodesma, and Fig. 5C and D also show a lot of 141Ce(III) located in cytoplasm. The results demonstrate that 141Ce(III) can enter into horseradish cells via plasmodesmata, and then it is mainly distributed in intercellular spaces, cell walls, plasmodesmata and cytoplasm, thus indicating that 141Ce(III) can be absorbed by leaves and then moved via apoplast vessels to the symplast. Similar behaviours of other ions have been also observed (Clarkson, 1993; Overall and Blackman, 1996; Ma and Carol, 2001).


Figure 5
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  		FIG. 5. Electron microscopic autoradiographs of 141Ce(III) in (A) the cell, (B) intercellular spaces, (C) near the cell wall, and (D) near mitochondria. Abbreviations: CW, cell wall; PM, plasma membrane; M, mitochondrion, Chl, chloroplast; ER, endoplasmic reticulum; PD, plasmodesmata.

 
In order to determine if the 141Ce(III) absorbed by horseradish would affect the distribution of other essential plant nutrients, the contents of K, Ca and Mg in the roots of control and treated plants were measured after 16 d (Fig. 6). Normal levels for these elements in plants were defined 3500–6600 mg kg–1 for K (Zottl and Hüttl, 1989), 2300–5000 mg kg–1 for Ca and 500–1300 mg kg–1 for Mg (Smidt, 1988). It can be seen from Fig. 6 that in control plants the mean contents of K, Ca and Mg in the roots were 4500, 3000 and 700 mg kg–1, respectively, which are similar to the normal levels of these elements in plants. However, the mean contents of K, Ca and Mg in the root of horseradish treated with 141Ce(III) were only 3000, 2000 and 250 mg kg–1, respectively, which is much lower than the normal values. The results indicate that when the content of 141Ce(III) is higher than the normal level of the plant, the metabolism of these macronutrients in horseradish would be disturbed, potentially leading to nutrient deficiency, inhibition of growth and reduced longevity (Lamppu and Huttunen, 2003).


Figure 6
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  		FIG. 6. The contents of K, Ca and Mg in roots of horseradish in control plants and those treated with 141Ce(III) (1000 mg L–1).

 


   CONCLUSIONS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
LITERATURE CITED
 
The distribution and translocation of a rare earth element, i.e. 141Ce(III), in horseradish were qualitatively and quantitatively investigated using radioisotope tracer techniques. The experimental results lead to the following conclusions.

After 141Ce(III) was applied to the surface of the leaf, it could be absorbed and transferred to the other organs of the plant. The uptake rates of 141Ce(III) varied with the different organs. The content of 141Ce(III) in horseradish organs followed the order of: roots > leaf-stalks > leaves.

The distribution of 141Ce(III) was different at different growth stages. The content of 141Ce(III) in the developing leaves was more than that in mature leaves, illustrating that the translocation of 141Ce(III) in horseradish is related to the metabolism of the plant.

141Ce(III) can penetrate through cell membranes and enter into the mesophyll cells via apoplastic and symplastic channels in the leaf or via plasmodesmata, and both extra- and intracellular deposition occurs.

The contents of K, Ca and Mg were decreased in horseradish treated with 141Ce(III), indicating that 141Ce(III) can disturb the metabolism of these macronutrients in the plant.


   ACKNOWLEDGMENTS
 
The authors are grateful for the financial support of the National Natural Science Foundation of China (No.20471030; No.30570323), and the Foundation of State Development and Reform Committee (No.IFZ2051210).


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 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
 LITERATURE CITED
 

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